Evaluating the Costs of Mosquito Resistance to Malaria Parasites

Abstract

Costly resistance mechanisms have been cited as an explanation for the widespread occurrence of parasitic infections, yet few studies have examined these costs in detail. A malaria-mosquito model has been used to test this concept by making a comparison of the fitness of highly susceptible lines of mosquitoes with lines that are resistant to infection. Malaria infection is known to cause a decrease in fecundity and fertility of mosquitoes; resistant mosquitoes were thus predicted to be fitter than susceptible ones. Anopheles gambiae were selected for refractoriness/resistance or for increased susceptibility to infection by Plasmodium yoelii nigeriensis. Additional lines that acted as controls for inbreeding depression were raised in parallel but not exposed to selection pressure. Selections were made in triplicate so that founder effects could be detected. Resistance mechanisms that were selected included melanotic encapsulation of parasites within 24 h postinfection and the complete disappearance of parasites from the gut. Costs of immune surveillance were assessed after an uninfected feed, and costs of immune deployment were assessed after exposure to infection and to infection and additional stresses. Mosquito survivorship was unaffected by either resistance to infection or by an increased burden of infection when compared with low levels of infection. In most cases reproductive fitness was equally affected by refractoriness or by infection. Resistant mosquitoes did not gain a fitness advantage by eliminating the parasites. Costs were consistently associated with larval production and egg hatch rate but rarely attributed to changes in blood feeding and never to changes in mosquito size. No advantages appeared to be gained by the offspring of resistant mosquitoes. Furthermore, we were unable to select for refractoriness in groups of mosquitoes in which 100% or 50% of the population were exposed to infection every generation for 22 generations. Under these selection pressures, no population had become completely refractory and only one became more resistant. Variations in fitness relative to control lines in different groups were attributed to founder effects. Our conclusion from these findings is that refractoriness to malaria is as costly as tolerance of infection. KeywordsAnopheles gambiae; fitness costs; innate immunity; malaria; mosquito; Plasmodium; refractoriness Despite their detrimental effects on the host, parasitic infections are extremely common (Esch and Fernandez 1993). This observation has led evolutionary ecologists to evoke life-history theories to explain why host traits for parasite resistance are not always selected. Immune defense is deemed to be costly, and thus supposed trade-offs exist with other fitness 2 E-mail: h.hurd@keele.ac.uk 3 E-mail: p.j.taylor@keele.ac.uk 4 E-mail: bia13@keele.ac.uk 5 E-mail: bia50@keele.ac.uk 6 E-mail: p.eggleston@keele.ac.uk UKPMC Funders Group Author Manuscript UKPMC Funders Group Author Manuscript UKPMC Funders Group Author Manuscriptcomponents. Th...

A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

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<span>Sporozoite Infection Rate and Identification of the Infective and Refractory Species of <i>Anopheles gambiae</i> (Giles) Complex</span>

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